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      The role of the hippocampus in flexible cognition and social behavior

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          Abstract

          Successful behavior requires actively acquiring and representing information about the environment and people, and manipulating and using those acquired representations flexibly to optimally act in and on the world. The frontal lobes have figured prominently in most accounts of flexible or goal-directed behavior, as evidenced by often-reported behavioral inflexibility in individuals with frontal lobe dysfunction. Here, we propose that the hippocampus also plays a critical role by forming and reconstructing relational memory representations that underlie flexible cognition and social behavior. There is mounting evidence that damage to the hippocampus can produce inflexible and maladaptive behavior when such behavior places high demands on the generation, recombination, and flexible use of information. This is seen in abilities as diverse as memory, navigation, exploration, imagination, creativity, decision-making, character judgments, establishing and maintaining social bonds, empathy, social discourse, and language use. Thus, the hippocampus, together with its extensive interconnections with other neural systems, supports the flexible use of information in general. Further, we suggest that this understanding has important clinical implications. Hippocampal abnormalities can produce profound deficits in real-world situations, which typically place high demands on the flexible use of information, but are not always obvious on diagnostic tools tuned to frontal lobe function. This review documents the role of the hippocampus in supporting flexible representations and aims to expand our understanding of the dynamic networks that operate as we move through and create meaning of our world.

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          Most cited references155

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          Emotional processing in anterior cingulate and medial prefrontal cortex.

          Negative emotional stimuli activate a broad network of brain regions, including the medial prefrontal (mPFC) and anterior cingulate (ACC) cortices. An early influential view dichotomized these regions into dorsal-caudal cognitive and ventral-rostral affective subdivisions. In this review, we examine a wealth of recent research on negative emotions in animals and humans, using the example of fear or anxiety, and conclude that, contrary to the traditional dichotomy, both subdivisions make key contributions to emotional processing. Specifically, dorsal-caudal regions of the ACC and mPFC are involved in appraisal and expression of negative emotion, whereas ventral-rostral portions of the ACC and mPFC have a regulatory role with respect to limbic regions involved in generating emotional responses. Moreover, this new framework is broadly consistent with emerging data on other negative and positive emotions. Published by Elsevier Ltd.
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            Deciding advantageously before knowing the advantageous strategy.

            Deciding advantageously in a complex situation is thought to require overt reasoning on declarative knowledge, namely, on facts pertaining to premises, options for action, and outcomes of actions that embody the pertinent previous experience. An alternative possibility was investigated: that overt reasoning is preceded by a nonconscious biasing step that uses neural systems other than those that support declarative knowledge. Normal participants and patients with prefrontal damage and decision-making defects performed a gambling task in which behavioral, psychophysiological, and self-account measures were obtained in parallel. Normals began to choose advantageously before they realized which strategy worked best, whereas prefrontal patients continued to choose disadvantageously even after they knew the correct strategy. Moreover, normals began to generate anticipatory skin conductance responses (SCRs) whenever they pondered a choice that turned out to be risky, before they knew explicitly that it was a risky choice, whereas patients never developed anticipatory SCRs, although some eventually realized which choices were risky. The results suggest that, in normal individuals, nonconscious biases guide behavior before conscious knowledge does. Without the help of such biases, overt knowledge may be insufficient to ensure advantageous behavior.
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              Loss of recent memory after bilateral hippocampal lesions.

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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                30 September 2014
                2014
                : 8
                : 742
                Affiliations
                [1] 1Department of Psychology and Beckman Institute, University of Illinois at Urbana-Champaign Urbana, IL, USA
                [2] 2Department of Communication Sciences and Disorders, University of Iowa Iowa City, IA, USA
                [3] 3Department of Neurology, Division of Behavioral Neurology and Cognitive Neuroscience, University of Iowa Iowa City, IA, USA
                Author notes

                Edited by: Richard Patterson, Emory University, USA

                Reviewed by: Stephen V. Shepherd, The Rockefeller University, USA; Jennifer D. Ryan, Rotman Research Institute, Canada

                *Correspondence: Rachael D. Rubin, Department of Psychology and Beckman Institute, University of Illinois at Urbana-Champaign, 405 N. Mathews Ave., Urbana, IL 61801, USA e-mail: rrubin2@ 123456illinois.edu

                This article was submitted to the journal Frontiers in Human Neuroscience.

                Article
                10.3389/fnhum.2014.00742
                4179699
                25324753
                e8808270-e7d9-42eb-b59c-208b62ea2dcb
                Copyright © 2014 Rubin, Watson, Duff and Cohen.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 08 June 2014
                : 03 September 2014
                Page count
                Figures: 3, Tables: 0, Equations: 0, References: 199, Pages: 15, Words: 14387
                Categories
                Neuroscience
                Review Article

                Neurosciences
                hippocampus,flexible cognition,social behavior,relational memory,amnesia
                Neurosciences
                hippocampus, flexible cognition, social behavior, relational memory, amnesia

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